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MacGuigan, D. J.

Publications and source records attributed to MacGuigan, D. J..

5 recordsLinked to original sources

A Lake Charr Pangenome Reveals Highly Conserved Ohnologs as Drivers of Phenotypic Diversity

Whole-genome duplication (WGD) is hypothesized to spur evolutionary diversification by producing genome-wide duplicate gene sets (Ohnologs) that are initially functionally redundant but can diverge markedly as the effects of relaxed selection accumulate over time. However, the underlying mechanisms remain unclear, in part because genomic studies often reconstruct Ohnolog evolution over millions of years, during which subsequent mutations can obscure deep-time signals. Investigating the relationship between Ohnolog evolution and diversification on a contemporary timescale offers clearer insights. We explore this relationship in Lake Charr (Salvelinus namaycush), where [~]10% of genes are retained highly conserved polyploid duplicates following the Salmonid-Specific Fourth Round WGD. Using 31 chromosome-level assemblies of Lake Charr from morphologically and ecologically diverse populations, joined into a pangenome graph, we characterized 189,555 structural variants (SVs) that were significantly less likely to affect genes retained as sequence-conserved Ohnolog pairs, nuancing the hypothesis that gene redundancy, relaxed selection, and functional diversification are intertwined. However, we found that SVs affecting such conserved Ohnologs may be potent drivers of adaptive evolution. Notably, we identified a putative 938-Kb interchromosomal translocation containing 25 genes with highly conserved Ohnologs in a paralogous (but untranslocated) genomic block. This putative translocation appears to have facilitated Ohnolog divergence in ankrd11 and hp, genes putatively linked to craniofacial and lipid metabolic diversity in sympatric Lake Superior morphs. This research reveals that conserved Ohnologs previously presumed to be redundant remain a reservoir for adaptive change.

genomics↗

Microsynteny Analysis Clarifies the Early Diversification of Cypriniform Fishes

While genomic data are powerfully informative for phylogenetic inference, traditional sequence-based analyses can be confounded by issues like homoplasy and incomplete lineage sorting, leaving deep nodes unresolved. Synteny, the conservation of gene order along a chromosome, presents a promising alternative source of phylogenetic information that is potentially less prone to these issues. Here we compare sequence and synteny phylogenetic phylogenomic approaches to unravel the evolutionary history of Cypriniformes, one of the most species-rich lineages of freshwater fishes. This clade has been plagued by uncertainty, particularly concerning the phylogenetic relationships between its four major subclades: Gyrinocheilidae (algae eaters), Catostomidae (suckers), Cobitoidei (loaches), and Cyprinoidei (minnows and carps). Phylogenomic approaches require high-quality genomic resources, which have been lacking for the family Gyrinocheilidae, a key lineage for understanding cypriniform evolution. To address this, we generated the first chromosome-level genome assembly and annotation for the Chinese Algae Eater (Gyrinocheilus aymonieri). We utilized this new genome along with 42 other fish genomes to conduct comprehensive phylogenomic analyses and compare results from sequence-based methods with a microsynteny-based approach. Although chromosome-level macrosynteny is broadly conserved among cypriniforms, we demonstrate that microsynteny has impressive power to resolve deep phylogenetic nodes. Both sequence-based and microsynteny-based analyses find that Gyrinocheilidae is the sister lineage to all other cypriniforms, resolving a long-standing phylogenetic point of contention. However, while sequence-based analyses provided weak support for the relationships among the remaining subclades, our microsynteny analysis revealed a novel and strongly supported sister relationship between Catostomidae and Cyprinoidei. This conclusion is supported by a 3- to 12-fold greater number of shared microsynteny clusters (synapomorphies) compared to the alternative topologies. We also demonstrate that microsynteny synapomorphies often arise from gene family expansions. Conservation of synteny concentrated in specific genomic regions may harbor the genomic underpinnings of the unique aspects of these clades and have played an important role in the evolutionary history of these taxa. Together, these results provide a robust phylogenomic backbone for Cypriniformes. More broadly, our findings highlight the power of microsynteny to resolve recalcitrant phylogenetic nodes where sequence data is uninformative, while also underscoring the critical importance of high-quality reference genomes, as our work also shows that including fragmented assemblies can lead to spurious results. Beyond phylogenomics, our results also provide a functional genomics glimpse into how conserved, clade-specific blocks of collinear genes (synteny synapomorphies) might contribute to what makes this hyperdiverse clade so unique and evolutionarily successful.

evolutionary biology↗

Spotty distributions: Spotted Gar (Lepisosteus oculatus) and Spotted Sucker (Minytrema melanops) range expansion in eastern Lake Erie

Natural range expansions in warm-water freshwater fishes are currently not well understood, but shifts in native species distributions can be influenced by many factors, including habitat restoration or degradation and climate change. Here, we provide empirical evidence of range expansions observed in two native freshwater fish species in Lake Erie: the Spotted Gar (Lepisosteus oculatus) and Spotted Sucker (Minytrema melanops). We confirmed our field identifications of L. oculatus and M. melanops using mtDNA barcoding. Maximum likelihood phylogenetic analyses reveal that our samples confidently resolve in the L. oculatus and M. melanops clades respectively, with additional identification support from BLAST searches. Notably, we found no correlation between the increased detection rate of both species and an increase in sampling effort when compared to previous records. Historically, eastern Lake Erie experienced habitat degradation through channelization, siltation, dredging, and toxification of sediments. We hypothesize that recent habitat remediation efforts have provided suitable habitat for both species to recolonize shallow waters with densely vegetated habitat (>90% substrate coverage). Both species are likely to continue their northern expansion as habitats are restored and climatic changes favor warm-water fishes.

zoology↗

Lacustrine speciation associated with chromosomal inversion in a lineage of riverine fishes

Geographic isolation is the primary driver of speciation in many vertebrate lineages. This trend is exemplified by North American darters, a clade of freshwater fishes where nearly all sister species pairs are allopatric and separated by millions of years of divergence. One of the only exceptions is the Lake Waccamaw endemic Etheostoma perlongum and its riverine sister species E. maculaticeps, which have no physical barriers to gene flow. Here we show that lacustrine speciation of E. perlongum is characterized by morphological and ecological divergence likely facilitated by a large chromosomal inversion. While Etheostoma perlongum is phylogenetically nested within the geographically widespread E. maculaticeps, there is a sharp genetic and morphological break coinciding with the lake-river boundary in the Waccamaw River system. Despite recent divergence, an active hybrid zone, and ongoing gene flow, analyses using a de novo reference genome reveal a 9 Mb chromosomal inversion with elevated divergence between E. perlongum and E. maculaticeps. This region exhibits striking synteny with known inversion supergenes in two distantly related fish lineages, suggesting deep evolutionary convergence of genomic architecture. Our results illustrate that rapid, ecological speciation with gene flow is possible even in lineages where geographic isolation is the dominant mechanism of speciation.

evolutionary biology↗

Historical contingency shapes adaptive radiation in Antarctic fishes

Adaptive radiation illustrates the links between ecological opportunity, natural selection, and the generation of biodiversity (1). Central to adaptive radiation is the association between a diversifying lineage and the evolution of key traits that facilitate the utilization of novel environments or resources (2, 3). However, is not clear whether adaptive evolution or historical contingency is more important for the origin of key phenotypic traits in adaptive radiation (4, 5). Here we use targeted sequencing of >250,000 loci across 46 species to examine hypotheses concerning the origin and diversification of key traits in the adaptive radiation of Antarctic notothenioid fishes. Contrary to expectations of adaptive evolution, we show that notothenioids experienced a punctuated burst of genomic diversification and evolved key skeletal modifications before the onset of polar conditions in the Southern Ocean. We show that diversifying selection in pathways associated with human skeletal dysplasias facilitates ecologically important variation in buoyancy among Antarctic notothenioid species, and demonstrate the sufficiency of altered trip11, col1a2 and col1a1 function in zebrafish (Danio rerio) to phenocopy skeletal reduction in Antarctic notothenioids. Rather than adaptation being driven by the cooling of the Antarctic (6), our results highlight the role of exaptation and historical contingency in shaping the adaptive radiation of notothenioids. Understanding the historical and environmental context for the origin of key traits in adaptive radiations provides context in forecasting the effects of climate change on the stability and evolvability of natural populations.

evolutionary biology↗